Laminarin stimulates single cell rates of sulfate reduction whereas oxygen inhibits transcriptomic activity in coastal marine sediment

• Published in: The ISME Journal Vol. 19; no. 1
• Main Authors: Lindsay, Melody R, D’Angelo, Timothy, Goodell, Elizabeth, Munson-McGee, Jacob H, Herring, Melissa, Budner, Michael, Brown, Julia M, Gavelis, Gregory S, Mascena, Corianna, Lubelczyk, Laura C, Poulton, Nicole J, Stepanauskas, Ramunas, Orcutt, Beth N, Emerson, David
• Format: Journal Article
• Language: English
• Published: England Oxford University Press 02.01.2025
• Subjects: Bacteria - genetics; Bacteria - metabolism; Electron Transport; Geologic Sediments - chemistry; Geologic Sediments - microbiology; Glucans - metabolism; Original; Oxidation-Reduction; Oxygen - metabolism; Single-Cell Analysis; Sulfates - metabolism; Transcriptome - drug effects; RedoxSensor green; laminarin; anaerobic respiration; coastal sediment; single-cell genomics; sulfate reduction; Chloroflexota
• ISSN: 1751-7362; 1751-7370; 1751-7370
• DOI: 10.1093/ismejo/wraf042

The chemical cycles carried out by bacteria and archaea living in coastal sediments are vital aspects of benthic ecology. These ecosystems are subject to physical disruption, which may allow for increased respiration and complex carbon consumption—impacting chemical cycling in this environment often thought to be a terminal place of deposition. We use the redox-enzyme sensitive probe RedoxSensor Green to measure rates of electron transfer physiology in individual sulfate reducer cells residing in anoxic sediment, subjected to transient exposure of oxygen and laminarin. We use index fluorescence activated cell sorting and single cell genomics sequencing to link those measurements to genomes of respiring cells. We measure per-cell sulfate reduction rates in marine sediments (0.01–4.7 fmol SO42− cell−1 h−1) and determine that cells within the Chloroflexota phylum are the most active in respiration. Chloroflexota respiration activity is also stimulated with the addition of laminarin, even in marine sediments already rich in organic matter. Evaluating metatranscriptomic data alongside this respiration-based technique, Chloroflexota genomes encode laminarinases indicating a likely ability to degrade laminarin. We also provide evidence that abundant Patescibacteria cells do not use electron transport pathways for energy, and instead likely carry out fermentation of polysaccharides. There is a decoupling of respiration-related activity rates from transcription, as respiration rates increase while transcription decreases with oxygen exposure. Overall, we reveal an active community of respiring Chloroflexota that cycles sulfate at potential rates of 23–40 nmol h−1 per cm3 sediment in incubation settings, and non-respiratory Patescibacteria that can cycle complex polysaccharides.